Abundance of wild prey modulates consumption of supplementary food in the Iberian lynx
José V. López-Bao *, Alejandro Rodríguez, Francisco Palomares
Department of Conservation Biology, Estación Biológica de Doñana (CSIC), Seville, Spain
Keywords:
Adaptive management Behavioural dependency Food supplementation Lynx pardinus
Prey abundance
Trophic ecology
a b s t r a c t
Food supplementation is increasingly used as a conservation tool. However, little is known about how much supplemental food is used by target populations or the degree to which the abundance of natural food affects the utilization of supplemental food. Long-term supplementation programmes could cause individuals to rely almost exclusively upon supplemental food and, consequently, lose some skills needed to forage efficiently on natural food. This may result in reduced fitness upon discontinuation of supple- mental food. The Iberian lynx (Lynx pardinus) preys almost exclusively upon European wild rabbits (Oryc- tolagus cuniculus), and some populations are thought to be food limited. We quantified the contribution of supplemented domestic rabbits, whose guard hairs could be distinguished from hairs of wild rabbits, to the diet of the Iberian lynx. We also examined whether the consumption of domestic rabbits varied with the availability of wild rabbits, and with the duration of exposure to supplemental food. Domestic rabbits made up over 50% of the diet. Consumption of domestic rabbits decreased non-linearly as the relative abundance of wild rabbits increased; however, this pattern was true only above a threshold density of one wild rabbit km—1. Below this threshold, supplementation was apparently strictly necessary to retain Iberian lynx. The consumption of domestic rabbits did not increase with the length of the supplementa- tion period. Lynx continued consuming wild rabbits proportionally to their abundance, suggesting lynx did not become dependent upon supplemental food. Understanding how the abundance of natural food modulates consumption of supplemental food may help to adjust supplementation schedules to food
availability and to the needs of the target populations.
1. Introduction
Providing supplemental food to wildlife is widely used as an experimental approach in the study of food limitation and its eco- logical consequences as well as a tool in the management of wild populations (Boutin, 1990; Putman and Staines, 2004; Jones and Reynolds, 2008; Robb et al., 2008). In a conservation context, sup- plementation is used to increase overall fitness by increasing pro- ductivity, survival, or both (Elliot et al., 2001; Schoech et al., 2008; López-Bao et al., 2010). However, unwanted side effects can arise, including increased obesity (Powlesland and Lloyd, 1994), disease and pathogen transmission (Miller et al., 2003; Jones and Reynolds,
2008), increased predation risk (Turner et al., 2008), and behav- ioural alterations (Reese and Kadlec, 1984; Boutin, 1990; Václav et al., 2003).
Since supplementary feeding is usually designed as a transi- tory measure to be employed only while levels of natural food
* Corresponding author. Address: Estación Biológica de Doñana, CSIC, c/Américo
Vespucio s/n, Isla de la Cartuja, 41092 Seville, Spain. Fax: +34 954 621 125.
E-mail address: (J.V. López-Bao).
remain depressed (López-Bao et al., 2008), a key goal should be to minimize the likelihood that a target population develops dependence upon supplemental food, implying the alteration or loss of foraging abilities. Under constant supply, animals may be- come increasingly reliant upon supplemental food (i.e. irrevers- ible dependence; Brittingham and Temple, 1992; Jones and Reynolds, 2008). In these instances, reducing the supply, whether gradually or precipitously may have negative effects. On the other hand, supplementation programs guided by the principles of adaptive management (Walters, 1986; Lee, 1999; Armstrong et al., 2007) dictate that the amount of supplemental food pro- vided should be adjusted to the abundance of natural food. Few studies have assessed the contribution of supplemental food to the diet of target populations (Brittingham and Temple, 1992; Partridge et al., 2001; Fleischer et al., 2003; Margalida et al.,
2009), but even fewer have assessed whether fluctuations in the abundance of natural food influence consumption of supple- mental food (Sauter et al., 2006).
The Iberian lynx (Lynx pardinus) is a specialist predator feeding almost exclusively upon European wild rabbits (Oryctolagus cunic- ulus; Delibes et al., 2000). Rabbit scarcity has been identified as a
:
major factor underlying the decline of lynx populations throughout its range (Rodríguez and Delibes, 2002). During the last 20 years, rabbit abundance has been extremely low at many sites within the Doñana area (Moreno et al., 2007), an area that supports one of the world’s two remaining Iberian lynx populations (Ferreras et al., 2010). In 2002, food supplementation was implemented as an emergency measure for lynx conservation and has proven useful for lynx retention under food-limited conditions (López- Bao et al., 2008, 2009). However, long-term food supplementation at a given locale, which by definition reduces the spatio-temporal variability that normally accompanies resource availability (López-Bao et al., 2008), could cause supplemented individuals to become dependent upon this resource. It is also conceivable that long-term supplementation could result in the loss of the skills that are needed to forage on wild rabbits. Were this the case, behaviourally dependent lynx may starve as a consequence of drastic variations or long disruptions in supplementation sched- ules, or when they leave supplemented areas.
In this study, we quantify the relative contributions of natural and supplemental food in the diet of the Iberian lynx. Specifically, we examined: (i) the importance of supplemental food in two lynx sub-populations with markedly different levels of natural prey abundance, (ii) whether consumption of supplemental food was influenced by temporal fluctuations in natural prey abundance, and (iii) whether consumption of supplemental food increased with exposure to food supplementation, as a sign of behavioural dependency.
2. Materials and methods
2.1. Study area and the supplementary feeding programme
We conducted our study in Doñana National Park, SW Spain (37°100 N, 6°230 W; Fig. 1). Lynx diet was studied in two well-de- fined lynx sub-populations called Vera (VE; 80 km2) and Coto del Rey (CR; 25 km2; Fig. 1), around 10 km apart, that have tradition- ally played the role of sources within the Doñana meta-population (Gaona et al., 1998). Sub-populations were isolated by unsuitable habitat (marsh; Fig. 1) and exchange of individuals occurred only rarely through natal dispersal (Ferreras, 2001). VE and CR differed markedly in rabbit abundance and lynx density. Over the last dec- ade, maximum lynx density in VE (5 ind 100 km—2) was lower than in CR (24 ind 100 km—2). Likewise, relative rabbit abundance in au- tumn, the low rabbit abundance period (Palomares, 2001), in VE was markedly lower (average number of rabbits per kilometer of transect ±SD = 0.07 ± 0.05 rabbits km—1; n transects = 7) than in CR (average number of rabbits per kilometer of transect
±SD = 4.08 ± 2.33 rabbits km—1; n transects = 6; Equipo de Seguimien-
to de Procesos Naturales – Estación Biológica de Doñana).
We provided live domestic rabbits kept in 4 x 4 m enclosures with walls 1.3 m high, hereby referred to as feeding stations. Sup- plementation was continuous and feeding stations were checked every other day to guarantee a regular and predictable source of food. In VE, food supplementation began in 2002, whereas it was implemented in CR beginning in 2006. Further details about the supplementation procedure are given by López-Bao et al. (2008). The provision of domestic rabbits was approved by the Regional Government of Andalusia through the implementation of the con- servation project LIFE-02NAT/8609.
Iberian lynx easily entered feeding stations, regularly used the supplemental food, and consumed almost all of the supplemental food in some frequently visited stations (López-Bao et al., 2008). In fact, during the study period, all animals identified living in VE and CR sub-populations used the supplemental food regularly (López-Bao et al., 2009).
2.2. Collection and analysis of lynx faeces
Lynx diet was studied by means of faecal analysis. Between Jan- uary 2005 and April 2007 we collected lynx faecal samples every
3 months. We searched for faeces along paths where Iberian lynx deposit most of their faeces (Robinson and Delibes, 1988).
Shape, size, colour, and smell are, in combination, diagnostic attributes of Iberian lynx scats. Some red fox (Vulpes vulpes) faeces could be wrongly attributed to lynx, but this occurs with very low frequency. DNA analyses showed that 99.7% of faeces (n = 369) were correctly assigned to lynx in the field (authors, unpublished data).
We were able to collect faecal samples in all breeding territo- ries. Each breeding territory holds one adult female, one adult male and one or more juveniles (Ferreras et al., 1997; López-Bao et al.,
2009). During the study period, VE contained two breeding territo- ries and CR contained three breeding territories (Fig. 1). Prelimin- ary results of a parallel study, in which lynx DNA was extracted from faecal samples collected with a similar sampling scheme, showed that faeces were produced by all individuals living in the sampled area (Rodríguez et al., 2009).
Faecal samples were broken, cleaned, and prey remains classi- fied and identified to the species level whenever possible (Debrot et al., 1982; Brown, 2003). We determined whether consumed rab- bits were wild or domestic on the basis of differences in the colour pattern of guard hairs found in faeces. Guard hairs of domestic rab- bits are known to be a single colour: white, black or brown (50%,
13% and 37%, respectively; n = 3560 supplemented rabbits). In con- trast, guard hairs of wild rabbits exhibit a characteristic tricoloured band at the tip (black at the base, tawny in the middle, and black at the apex). We used a 10x binocular lens to distinguish between the two types of rabbits.
2.3. Availability of wild rabbits
Rabbit abundance shows temporal fluctuations along the an- nual cycle with a low rabbit abundance period in autumn and a high rabbit abundance period in spring (Palomares, 2001; Palomares et al., 2001). We estimated relative rabbit abundance at each of the two study sites by counting rabbits from a vehicle along fixed transects (>10 km, one fixed transect per area:
14.7 km in VE and 16.2 km in CR) 1 h before dusk (when rabbit activity is least influenced by seasonal and environmental factors; Villafuerte et al., 1993) on three consecutive days each month (Moreno et al., 2007). Transects were conducted along paths of similar characteristics, guaranteeing a consistent wide and stable sampling area: a 10-m belt on each side of the transects. We used the highest count for the 3 days to calculate a monthly index of rel- ative abundance (index of abundance; henceforth, IA) for months during which faeces were collected. The IA was expressed as the total number of rabbits counted per kilometer of transect. This method to estimate relative rabbit abundance and their temporal fluctuations has been frequently used in the Doñana area (Moreno et al., 2007).
2.4. Data analyses
We calculated the frequency of occurrence of domestic rabbits in the lynx diet. For each faecal sample we recorded the occurrence of wild rabbits and the occurrence of domestic rabbits, and ex- pressed them as two binary variables. We used generalized linear models with binomial error and logit-link to analyse the influence of the area and relative abundance of wild rabbits on the occur- rence of each type of rabbit in the lynx diet. We included the time elapsed (months) between the date when supplemental food was first provided in each area and the date when each faecal sample
Fig. 1. Distribution of the two lynx sub-populations studied in the Doñana area, VE and CR (80 km2 and 25 km2 respectively), SW Spain. Doñana National Park is highlighted in dark grey (dunes and scrubland) and clear grey (marsh). Spatial location of all the breeding territories existing in both sub-populations (two in VE and three in CR) during the study period are shown as fixed kernel home ranges using 90% of positions of resident adult females (black polygons). Black points denote the spatial location of all faeces
collected in this study.
was collected as a covariate in the models to test for variations in consumption of supplemental food over time. All statistical analy- ses were performed using the R statistical software V.2.8.0 (R Development Core Team, 2008).
3. Results
A total of 323 faeces samples were collected, 158 in VE and 165 in CR. Overall, only 1.5% of faeces contained prey items other than rabbits: red-legged partridge (Alectoris rufa), red deer (Cervus ela- phus) and ducks (Anas spp.). Out of 323 faeces, 212 (65%) contained only hair of domestic rabbits, 93 (29%) had only hair of wild rab- bits, and 18 (6%) had hair of both types of rabbits. The proportion of faeces containing hair of domestic rabbits accounted for >50% in both areas, but its proportion in VE (83%) was significantly higher (v2 = 21.19, df = 1, P < 0.001) than its proportion in CR (59%). Hair of wild rabbits appeared in 27% and 41% of scats in VE and CR, respectively.
Overall, the use of supplemental food was influenced by the rel- ative abundance of wild rabbits. In spite of this, the consumption of domestic rabbits in VE was relatively constant over time (mean monthly proportion in the diet = 0.86, range = 0.72–1.00), irrespec- tive of the numbers of wild rabbits which did not statistically change over the course of the study (v2 = 1.53, df = 1, P = 0.216; Fig. 2) and remained below the 1 rabbit km—1 (range 0–0.91 rabbits km—1). However, in CR, IA varied in the range of 1.5–15.0 rabbits km—1, and the proportion of domestic rabbits in the lynx diet also varied widely around a mean of 0.56 (range = 0.25–
0.83). The relationship between consumption of domestic rabbits and relative abundance of wild rabbits was negative and had a steep slope (Fig. 2). Abundance of wild rabbits began to negatively influence the consumption of supplemental food above a threshold of one rabbit km—1, and this effect was significant (v2 = 5.55, df = 1, P = 0.019). Our model predicted an equal consumption of wild and domestic rabbits when the relative abundance of wild rabbits was about seven rabbits km—1 (Fig. 2). Consequently, the frequency of occurrence of wild rabbits in the lynx diet was only modulated
1.0
0.8
0.6
0.4
0.2
0.0
n.s
n.s
hypothesis that lynx prefer wild rabbits was also supported by the fact that as the abundance of wild rabbits increased, lynx con- sumed a greater proportion of wild rabbits (see Fig. 2). This possi- ble preference for wild rabbits, even when the alternative prey is so similar, could be associated with a lack in some important nutri- tional component in the supplied food or with unknown costs of visiting feeding stations (e.g. competitive interactions with other lynx; López-Bao et al. (2009). In fact, we tend to believe that with- out food supplementation the lynx may have abandoned the VE area.
Although domestic rabbits made up a considerable fraction of the lynx diet, in CR consumption of supplemental food greatly var- ied over time. The role that supplemental food played in the lynx diet was apparently modulated by the abundance of wild prey.
The consumption of domestic rabbits decreased with increasing
0.00.20.40.60.81.0
Relative abundance of wild rabbits (rabbits km-1)
1.0
abundance of wild rabbits. However, our results suggest that this prey shift only occurs above a threshold value of wild rabbit abun- dance. Below this threshold, lynx seem to be compelled to survive upon supplementary food.
Feeding stations were operative between 2 and 5 years (López-
0.8
0.6
0.4
0.2
0.0
P < 0.05
P < 0.05
246810121416
Relative abundance of wild rabbits (rabbits km-1)
Bao et al., 2008, 2009). After such a long exposure to supplemen- tary food Iberian lynx continued to prey upon wild rabbits and we found no sign that they progressively reduced the intake of nat- ural food over time. Lynx seemed to be able to discriminate be- tween natural and artificial food (Sauter et al., 2006), with prey choice being determined by wild rabbit abundance. From this we infer that, overall, lynx apparently did not lose the skills necessary to forage efficiently on wild rabbits. We conclude that the hypoth- esis that food supplementation promotes high levels of behav- ioural dependency in the Iberian lynx was not supported.
There have been many efforts to increase wild rabbit densities in Doñana through habitat management and rabbit translocations to aid conservation of the Iberian lynx (Moreno and Villafuerte,
1995; LIFE, 2002; Delibes-Mateos et al., 2009). To date, most of
Fig. 2. Predicted frequency of occurrence of wild (dashed line) and supplemented rabbits (solid line) in lynx faeces against the relative abundance of wild rabbits in VE (upper panel) and CR (lower panel). Note that patterns with a significant slope are shown. ns = non significant.
by their density in CR (v2 = 4.50, df = 1, P = 0.034 for CR and
v2 = 0.01, df = 1, P = 0.971 for VE; Fig. 2).
The length of the period that lynx were exposed to food supple- mentation had no significant effect on the proportion of domestic rabbits in the lynx diet (v2 = 0.01, df = 1, P= 0.968 for CR; v2 = 2.59, df = 1, P= 0.107 for VE).
4. Discussion
The fact that supplemental rabbits were an important resource for the Iberian lynx in both areas may be explained by two lines of reasoning. Firstly, a high level of consumption of domestic rabbits may reflect the severe scarcity of wild rabbits at many sites in the Doñana area, particularly in VE (Moreno et al., 2007), combined with the strict trophic specialization of the Iberian lynx (Delibes et al., 2000). Secondly, all else being equal, predators take the most vulnerable prey (Quinn and Cresswell, 2004). Therefore, high con- sumption levels of supplemental food may arise in part due to the capture of domestic rabbits in small enclosures requiring lower foraging costs compared to seeking wild rabbits at very low densi- ties. This might be especially true in VE.
As previously suggested by López-Bao et al. (2008), we found that lynx continued to feed on wild rabbits, even in VE where the supplemented rabbits were an ecological necessity. This suggests that lynx may prefer to feed on natural food where available. The
these attempts have been relatively unsuccessful, with results being only satisfactory on a small scale (Moreno et al., 2004). We recommend the use of supplementary feeding during periods where the relative density of wild rabbits within lynx territories does not reach at least a value of IA = 1 rabbit km—1. As wild rabbit density increases above this threshold value, supplementation may still be necessary but schedules may be adjusted to rabbit abun- dance and the energetic demands of lynx (López-Bao et al., 2008,
2009) following an adaptive management approach (Walters,
1986; Lee, 1999; Armstrong et al., 2007). To adapt supplementa- tion to wild rabbit abundance efficient methods to monitor rabbit abundance and its variations in the short and mid-term is needed, as well as at different spatial scales.
Acknowledgements
This research was funded by the Spanish Ministry of Education and Science (project CGL2004-00346/BOS), the Spanish Ministry of the Environment under the National Parks research programme (Grant-17/2005), and BP-Oil Spain. The Consejería de Medio Ambi- ente (Junta de Andalucía, JA) partially financed the supplementary feeding programme under the project LIFE-02NAT/8609. Land-Ro- ver España S.A. kindly lended the vehicles for this work. JVLB was supported by a FPU fellow (Ministry of Education).
References
Armstrong, D.P., Castro, I., Griffiths, R., 2007. Using adaptive management to determine requirements of reintroduced reintroduced populations: the case of the New Zealand Hihi. Journal of Applied Ecology 44, 953–962.